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Research ArticleGENETICS, GENOMICS, AND MOLECULAR EVOLUTION
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Carbohydrate-Active Enzymes Involved in the Secondary Cell Wall Biogenesis in Hybrid Aspen

Henrik Aspeborg, Jarmo Schrader, Pedro M. Coutinho, Mark Stam, Åsa Kallas, Soraya Djerbi, Peter Nilsson, Stuart Denman, Bahram Amini, Fredrik Sterky, Emma Master, Göran Sandberg, Ewa Mellerowicz, Björn Sundberg, Bernard Henrissat, Tuula T. Teeri
Henrik Aspeborg
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Jarmo Schrader
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Pedro M. Coutinho
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Mark Stam
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Åsa Kallas
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Soraya Djerbi
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Peter Nilsson
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Stuart Denman
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Bahram Amini
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Fredrik Sterky
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Emma Master
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Göran Sandberg
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Ewa Mellerowicz
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Björn Sundberg
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Bernard Henrissat
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Tuula T. Teeri
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Published March 2005. DOI: https://doi.org/10.1104/pp.104.055087

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    Figure 1.

    Clustering using self-organizing maps of 450 genes. Genes with less than two valid data points in sections C to E or with a signal less than 2-fold higher in D than in A to C and E were filtered out.

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    Figure 2.

    Phylogenetic analysis of plant GTs from family GT8. Profile-aligned Populus sequences are in bold, and partial sequences are indicated. Subfamilies with at least one characterized enzyme are outlined by a thick black line and those without defined activities by a thin gray line.

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    Figure 3.

    Phylogenetic analysis of plant GTs from family GT43. Legend as in Figure 2.

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    Figure 4.

    Phylogenetic analysis of plant GTs from family GT47. Legend as in Figure 2.

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    Figure 5.

    Phylogenetic analysis of plant GTs from family GT61. Legend as in Figure 2.

Tables

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    Table I.

    Strictly D-specific genes encoding CAZymes: a selection of genes that passed both filter I and filter II

    Ratios are presented in log2 scale, and log2 ratios >1 are in bold.

    GeneaSequenceaESTa13.5 K Arraya3 K ArraybXy versus Phc
    ABCDE
    PttCesA1FLA064P24U−6.41−5.79−0.301.26−0.58Yes5.66
    PttCesA1FLG109P08Y−4.79−4.41−0.181.79−0.70NA5.30
    PttCesA3-1FLA040P09U−4.77−4.330.541.75−1.64Yes5.04
    PttCesA3-2FLG097P01U−6.02−5.45−0.201.81−0.32NA5.27
    PttCesA3-2FLG103P13Y−5.88−5.59−0.321.34−0.29NA5.44
    PttCesA9PartialG072P74Y−6.03−5.46−0.082.62−1.07NA6.11
    PttCesA9PartialG072P58Y−2.03−1.700.031.480.33NA4.47
    PttGT2APartialB005P05U−4.77−4.77−0.592.060.01Yes5.89
    PttGT8BFLA065P67U−5.91−5.54−1.322.24−1.99Yes6.51
    PttGT8BFLG069P14Y−5.89−5.11−1.282.35−1.90NA6.65
    PttGT8CFLA073P75U−4.74−4.900.332.04−1.61Yes5.66
    PttGT8DPartialB004P07U−6.69−6.26−1.651.98−0.62Yes6.25
    PttGT8DPartialG069P39Y−4.41−4.45−1.482.30−0.58NA5.93
    PttGT8EFLG079P18Y−1.39−1.110.231.98−2.19NA2.71
    PttGT8EFLUB22CPE03−0.81−1.100.211.95−2.51NA3.19
    PttGT8FPartialG069P06Y−2.39−2.07−0.742.36−0.47NA4.98
    PttGT31APartialG133P32Y−2.14−1.970.862.02−2.03NA3.10
    PttGT43AFLB002P16U−4.31−4.250.331.79−3.59Yes4.69
    PttGT43BFLA027P19U−5.05−4.100.371.94−2.32Yes4.76
    PttGT47AFLA004P36U−5.16−5.24−0.671.25−2.03Yes5.06
    PttGT47AFLA005P12U−4.58−4.75−0.661.60−2.05Yes4.89
    PttGT47AFLA012P11U−4.71−4.71−0.791.61−1.89Yes5.26
    PttGT47AFLG106P73.3pR−4.06−3.90−0.572.02−1.96NA4.36
    PttGT47AFLG072P66.3pR−3.36−2.84−0.382.29−1.42NA1.33
    PttGT47CFLA045P41U−4.28−4.03−0.421.95−0.20Yes5.29
    PttGT47CFLA018P14U−2.92−2.80−0.281.950.18Yes5.12
    PttGT47CFLG099P90Y−1.49−0.950.231.66−0.31NA4.51
    PttGT47CFLI042P36P−1.52−1.820.062.390.15NA4.18
    PttGT47DPartialG124P64Y−1.10−0.86−0.041.88−1.16NA2.56
    PttCel9AFLA064P06U−2.35−1.940.021.490.15Yes2.69
    PttXyn10AFLA020P21U−2.53−1.76−0.492.000.60Yes3.43
    PttGH17APartialG083P33Y−0.48−0.650.101.55−0.26NA−1.87
    PttGH19AFLA044P10U−6.73−6.42−1.150.95−0.37Yes6.60
    PttGH19AFLG066P41.5pR−6.27−5.75−1.161.46−0.74NA5.93
    PttGH19AFLG063P44.3pR−3.89−3.49−1.131.41−0.63NA4.64
    PttGH28APartialA060P67U−1.85−1.87−0.041.550.43Yes3.52
    PttBGal35APartialA066P74U0.02−0.20−0.421.71−1.58Yes1.19
    PttGH51APartialF025P61Y−1.77−1.80−1.552.62−0.73NA3.49
    • ↵a Several genes are represented by more than one EST on the arrays. FL, Full-length sequence.

    • ↵b Data published in Hertzberg et al. (2001). Yes/no, Gene was/was not up-regulated in the D zone; NA, not available because the EST was not represented on the array.

    • ↵c Expression data for rows 1 to 7 have been published in Djerbi et al. (2004). Xy, Xylem; Ph, phloem.

    • View popup
    Table II.

    Genes encoding CAZymes highly expressed during secondary cell wall formation: a selection of genes that passed filter I but did not fulfill the requirements of filter II

    Ratios are presented in log2 scale, and log2 ratios >1 are in bold.

    GeneaSequenceaESTa13.5 K Arraya3 K ArraybXy versus Phc
    ABCDE
    PttCesA2FLF120P33Y−0.30−0.820.701.160.87NA0.63
    PttCesA2FLA020P56U−0.34−0.850.580.940.71No0.63
    PttGT8APartialA002P51.3pR−3.44−1.280.221.751.07Yes3.75
    PttGT8APartialA002P78U−3.46−1.38−0.011.420.91Yes3.53
    PttGT8GPartialA068P23U−0.350.040.481.08−1.39No1.22
    PttGT8GPartialF056P93Y−0.190.300.710.82−0.63NA0.41
    PttGT8HPartialG091P40Y−1.02−0.65−0.041.041.84NA2.34
    PttGT14AFLA002P61U−1.89−1.910.671.600.34Yes3.91
    PttGT14BFLB005P04U−2.75−1.150.921.34−1.64Yes2.57
    PttGT31BPartialG108P23Y−1.59−1.100.621.510.20NA2.15
    PttGT47BFLA006P34U−1.51−1.23−0.261.95−0.33Yes3.25
    PttGT61APartialG123P20Y−0.410.140.851.020.29NA0.64
    PttGT61APartialA020P80U−0.530.140.690.800.03No0.59
    PttXET16LPartialUB27CPD070.00−0.530.021.421.10NA−0.11
    PttBGal35BPartialG079P88Y−3.55−3.720.691.230.94NA3.34
    PttBGal35BPartialG107P47Y−3.48−4.200.751.241.07NA3.16
    • ↵a Several genes are represented by more than one EST on the arrays.

    • ↵b Data published in Hertzberg et al. (2001). Yes/no, Gene was/was not up-regulated in the D zone; NA, not available because the EST was not represented on the array.

    • ↵c Expression data for rows 1 and 2 have been published in Djerbi et al. (2004). Xy, Xylem; Ph, phloem.

    • View popup
    Table III.

    Closest Arabidopsis homologs to the Populus CAZymes and published secondary wall-related expression data from other relevant plants

    GeneHomologPublished Expression DataCotton
    ArabidopsisArabidopsisaZinnia
    PttGT2A CSLAt5g03760Demura et al. (2002)
    PttCesA1At5g44030Milioni et al. (2002)Pear et al. (1996)
    PttCesA2At4g39350Li et al. (2002)
    PttCesA3-1At4g18780S1 and S4Demura et al. (2002)Pear et al. (1996)
    PttCesA3-2At4g18780S1 and S4Demura et al. (2002)Pear et al. (1996)
    PttCesA9At5g17420S1
    PttGT8AAt4g33330
    PttGT8BAt3g18660Demura et al. (2002)
    PttGT8CAt3g18660Demura et al. (2002)
    PttGT8DAt5g54690
    PttGT8EAt1g19300
    PttGT8FAt1g19300
    PttGT8GAt3g02350
    PttGT8HAt3g62660
    PttGT14AAt3g03690
    PttGT14BA1gt71070
    PttGT31AAt3g14960
    PttGT31BAt1g05170S1Demura et al. (2002)
    PttGT43AAt2g37090Zhao et al. (2001)
    PttGT43BAt2g37090S1 and S4
    PttGT47AAt1g27440
    PttGT47BAt3g45400
    PttGT47CAt2g28110Demura et al. (2002)
    PttGT47DAt5g61840
    PttGT61AAt5g55500
    PttCel9AAt5g49720S1Demura et al. (2002)
    PttXyn10AAt1g58370Demura et al. (2002)
    PttGH16LAt1g14720S1Ji et al. (2003)
    PttGH17AAt4g14080
    PttGH19AAt3g16920
    PttGH28AAt3g42950
    PttBGal35AAt5g63800Zhao et al. (2001)
    PttBGal35BAt3g13750
    PttGH51AAt3g10740Demura et al. (2002)
    • ↵a Data published by Oh et al. (2003). S1, Xylem up-regulated genes; S4, control up-regulated genes.

    • View popup
    Table IV.

    Percentage identities/positives of the protein sequences of CesA proteins identified in poplar, Arabidopsis, barley, and rice

    Gene sequences were retrieved from the Stanford Web site (http://cellwall.stanford.edu). Boldface indicates genes involved in secondary cell wall synthesis (data from Taylor et al., 2000, 2003; Joshi, 2003; Tanaka et al., 2003; Burton et al., 2004; Djerbi et al., 2004). At, Arabidopsis; Ptr, P. tremuloides; Hv, barley; Os, rice.

    GeneP. tremula × tremuloides (Ptt)/P. trichocarpa
    CesA1CesA2CesA3-1CesA3-2CesA4CesA5aCesA7aCesA8aCesA9a
    AtCesA162/7462/7461/7161/7261/7368/7868/8083/8962/72
    AtCesA259/7074/8157/7156/6977/8362/7463/7661/7361/72
    AtCesA363/7462/7761/7260/7162/7681/8779/8668/7865/74
    AtCesA472/7958/7064/7562/7357/6961/7162/7361/7261/70
    AtCesA560/7273/8056/6957/7075/8063/7563/7561/7360/71
    AtCesA661/7376/8456/6957/7079/8563/7563/7561/7360/71
    AtCesA762/7362/7461/7261/7261/7365/7466/7663/7481/86
    AtCesA864/7457/7080/8779/8756/6959/7060/7260/7160/71
    AtCesA959/7276/8456/6956/7077/8464/7462/7661/7360/71
    AtCesA1060/7360/7360/7259/7160/7266/7767/7979/8560/71
    PtrCesA163/7456/6991/9392/9255/6957/6959/7159/7059/71
    PtrCesA262/7162/7360/7258/7061/7265/7566/7663/7388/89
    PtrCesA385/8557/6963/7460/7057/6760/7163/7361/7262/71
    PtrCesA461/7363/7660/7160/7261/7468/7867/7894/9463/74
    PtrCesA560/7162/7458/6957/6963/7490/9080/8567/7764/72
    PtrCesA661/7266/7660/7258/6966/7666/7666/7765/7663/73
    PtrCesA760/7076/8255/6755/6888/8865/7765/7862/7462/73
    HvCesA161/7162/7558/7058/7061/7375/8376/8467/7763/72
    HvCesA2b60/7165/7558/7156/6865/7565/7564/7663/7562/72
    HvCesA3b61/7261/7459/7158/7061/7376/8277/8467/7664/73
    HvCesA4b71/7661/7267/7664/7160/7263/7364/7466/7464/72
    HvCesA5/7b68/7965/7978/8578/8665/7967/7967/7967/7865/76
    HvCesA662/7462/7461/7260/7162/7367/7768/7980/8662/72
    HvCesA8b68/8172/8171/8268/8071/8178/8578/8474/8382/85
    OsCesA162/7361/7261/7159/7061/7268/7869/8081/8762/72
    OsCesA262/7363/7659/7059/7163/7578/8478/8468/7865/74
    OsCesA362/7368/7958/7058/7067/7866/7665/7666/7764/74
    OsCesA462/7367/8174/8174/8166/8060/7261/7360/7159/70
    OsCesA562/7368/7858/7058/7068/7866/7665/7665/7764/74
    OsCesA661/7266/7658/7157/7066/7666/7665/7864/7662/73
    OsCesA770/7657/6962/7260/6956/6660/7062/7362/7162/71
    OsCesA861/7163/7659/7058/7062/7378/8478/8468/7764/73
    OsCesA9b71/8377/8671/8470/8377/8574/8475/8571/8271/82
    • ↵a Full-length sequences retrieved from the genome sequence of P. trichocarpa.

    • ↵b Partial sequences.

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Carbohydrate-Active Enzymes Involved in the Secondary Cell Wall Biogenesis in Hybrid Aspen
Henrik Aspeborg, Jarmo Schrader, Pedro M. Coutinho, Mark Stam, Åsa Kallas, Soraya Djerbi, Peter Nilsson, Stuart Denman, Bahram Amini, Fredrik Sterky, Emma Master, Göran Sandberg, Ewa Mellerowicz, Björn Sundberg, Bernard Henrissat, Tuula T. Teeri
Plant Physiology Mar 2005, 137 (3) 983-997; DOI: 10.1104/pp.104.055087

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Carbohydrate-Active Enzymes Involved in the Secondary Cell Wall Biogenesis in Hybrid Aspen
Henrik Aspeborg, Jarmo Schrader, Pedro M. Coutinho, Mark Stam, Åsa Kallas, Soraya Djerbi, Peter Nilsson, Stuart Denman, Bahram Amini, Fredrik Sterky, Emma Master, Göran Sandberg, Ewa Mellerowicz, Björn Sundberg, Bernard Henrissat, Tuula T. Teeri
Plant Physiology Mar 2005, 137 (3) 983-997; DOI: 10.1104/pp.104.055087
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Plant Physiology: 137 (3)
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